Trace Fear Conditioning Differentially Modulates Intrinsic Excitability of Medial Prefrontal Cortex–Basolateral Complex of Amygdala Projection Neurons in Infralimbic and Prelimbic Cortices

Song, Chenghui; Ehlers, Vanessa L.; Moyer, James R.

doi:10.1523/jneurosci.2329-15.2015

Cited by 85 publications

(83 citation statements)

References 72 publications

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“…In contrast to our findings, a recent study found that trace fear conditioning increases the excitability of IL layer V neurons projecting to the amygdala (Song et al, 2015). There are several differences between the studies that could contribute to the discrepancy.…”

Section: Discussioncontrasting

confidence: 99%

Contextual fear conditioning depresses infralimbic excitability

Soler-Cedeño

Cruz

Criado‐Marrero

et al. 2016

Neurobiology of Learning and Memory

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Patients with posttraumatic stress disorder (PTSD) show hypo-active ventromedial prefrontal cortices (vmPFC) that correlate with their impaired ability to discriminate between safe and dangerous contexts and cues. Previously, we found that auditory fear conditioning depresses the excitability of neurons populating the homologous structure in rodents, the infralimbic cortex (IL). However, it is undetermined if IL depression was mediated by the cued or contextual information. The objective of this study was to examine whether contextual information was sufficient to depress IL neuronal excitability. After exposing rats to context-alone, pseudoconditioning, or contextual fear conditioning, we used whole-cell current-clamp recordings to examine the excitability of IL neurons in prefrontal brain slices. We found that contextual fear conditioning reduced IL neuronal firing in response to depolarizing current steps. In addition, neurons from contextual fear conditioned animals showed increased slow afterhyperpolarization potentials (sAHPs). Moreover, the observed changes in IL excitability correlated with contextual fear expression, suggesting that IL depression may contribute to the encoding of contextual fear.

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Section: Discussioncontrasting

confidence: 99%

Contextual fear conditioning depresses infralimbic excitability

Soler-Cedeño

Cruz

Criado‐Marrero

et al. 2016

Neurobiology of Learning and Memory

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“…Altogether, these data indicate that mAHP is increased from 1 to 10 d of training in FosGFP Ϫ neurons, but not in FosGFP ϩ neurons, which corresponds with our previously observed decrease of intrinsic excitability in FosGFP Ϫ neurons from 1 to 10 d of training. SK channels are known to contribute to mAHP magnitude in cortical neurons (Alger et al, 1994;Sah and Faber, 2002). We used the selective SK channel antagonist apamin to study the role of SK channels in modulating the firing rate of FosGFP Ϫ PLC neurons from only the test group rats.…”

Section: Plc Neurons After Food Self-administrationmentioning

confidence: 99%

“…One possible scenario is that different neuronal ensembles intermingle within PLC that encode separate learned associations or memories (Warren et al, 2016). This seems likely given the diverse role of PLC in attentional allocation, contextual encoding, and rewarding and aversive learning (Watanabe, 1996;Schall et al, 2002;Fujii and Graybiel, 2003;Euston et al, 2012;Sharpe and Killcross, 2014;Pinto and Dan, 2015). In support of this idea, recently, we demonstrated a critical role of infralimbic cortex (ILC) neuronal ensembles in both operant learning and extinction of the operant response (Warren et al, 2016).…”

Section: Intrinsic Excitability Alterations Within Fos-expressing Neumentioning

confidence: 99%

Bidirectional Modulation of Intrinsic Excitability in Rat Prelimbic Cortex Neuronal Ensembles and Non-Ensembles after Operant Learning

Whitaker¹,

Warren²,

Vènniro³

et al. 2017

J. Neurosci.

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Learned associations between environmental stimuli and rewards drive goal-directed learning and motivated behavior. These memories are thought to be encoded by alterations within specific patterns of sparsely distributed neurons called neuronal ensembles that are activated selectively by reward-predictive stimuli. Here, we use the Fos promoter to identify strongly activated neuronal ensembles in rat prelimbic cortex (PLC) and assess altered intrinsic excitability after 10 d of operant food self-administration training (1 h/d). First, we used the Daun02 inactivation procedure in male FosLacZ-transgenic rats to ablate selectively Fos-expressing PLC neurons that were active during operant food self-administration. Selective ablation of these neurons decreased food seeking. We then used male FosGFPtransgenic rats to assess selective alterations of intrinsic excitability in Fos-expressing neuronal ensembles (FosGFP ϩ ) that were activated during food self-administration and compared these with alterations in less activated non-ensemble neurons (FosGFP Ϫ ). Using whole-cell recordings of layer V pyramidal neurons in an ex vivo brain slice preparation, we found that operant self-administration increased excitability of FosGFP ϩ neurons and decreased excitability of FosGFP Ϫ neurons. Increased excitability of FosGFP ϩ neurons was driven by increased steady-state input resistance. Decreased excitability of FosGFP Ϫ neurons was driven by increased contribution of small-conductance calcium-activated potassium (SK) channels. Injections of the specific SK channel antagonist apamin into PLC increased Fos expression but had no effect on food seeking. Overall, operant learning increased intrinsic excitability of PLC Fosexpressing neuronal ensembles that play a role in food seeking but decreased intrinsic excitability of Fos Ϫ non-ensembles.

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“…Within the mPFC, the infralimbic (IL) and prelimbic (PL) cortices are intimately implicated in fear extinction and fear acquisition respectively 21 . The IL and PL send strong inputs to the amygdala and may gate inputs from the BLA into the CeA 39,21,40 . The NAc and BLA have robust reciprocal connections.…”

Section: Background On Circuitry and Fearmentioning

confidence: 99%

Bridging the Gap : Towards a cell-type specific understanding of neural circuits underlying fear behaviors

McCullough

Morrison

Ressler

2016

Neurobiology of Learning and Memory

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Fear and anxiety-related disorders are remarkably common and debilitating, and are often characterized by dysregulated fear responses. Rodent models of fear learning and memory have taken great strides towards elucidating the specific neuronal circuitries underlying the learning of fear responses. The present review addresses recent research utilizing optogenetic approaches to parse circuitries underlying fear behaviors. It also highlights the powerful advances made when optogenetic techniques are utilized in a genetically defined, cell-type specific, manner. The application of next-generation genetic and sequencing approaches in a cell-type specific context will be essential for a mechanistic understanding of the neural circuitry underlying fear behavior and for the rational design of targeted, circuit specific, pharmacologic interventions for the treatment and prevention of fear-related disorders.

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Trace Fear Conditioning Differentially Modulates Intrinsic Excitability of Medial Prefrontal Cortex–Basolateral Complex of Amygdala Projection Neurons in Infralimbic and Prelimbic Cortices

Cited by 85 publications

References 72 publications

Contextual fear conditioning depresses infralimbic excitability

Contextual fear conditioning depresses infralimbic excitability

Bidirectional Modulation of Intrinsic Excitability in Rat Prelimbic Cortex Neuronal Ensembles and Non-Ensembles after Operant Learning

Bridging the Gap : Towards a cell-type specific understanding of neural circuits underlying fear behaviors

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